Mosquito-borne diseases are a major public health concern in the Caribbean. Domestic water-storage containers are preferred breeding habitats for synanthropic mosquito species, among which Aedes aegypti stands out due to its role in arbovirus transmission. To determine the microenvironmental features associated with container-dwelling mosquitoes, a house-to-house cross-sectional entomological survey was carried out in 9 Dominican provinces affected by Zika virus in 2016. All containers with the potential to store water were sampled, all immature mosquitoes were collected, and information on the type, capacity, volume of stored water, building material, presence of flowers, and house location was documented. The specimens were identified and larval indices (House index [HI], Container index [CI], Breteau index [BI], and Ae. aegypti Breeding Percentage) were applied. A total of 665 dwellings were surveyed across 30 neighborhoods. A total of 1,420 water-filled container habitats were sampled, 19.3% of which harbored immature mosquitoes of 5 species, including 4 important vectors. The dominance of Ae. aegypti was marked, as it was present in all sampled neighborhoods, inhabiting 272 containers (19.1%). Larval indices were higher than the threshold values accepted (5% for the HI and BI, and 3% for the CI) in almost all neighborhoods. The presence of Aedes spp. was associated with the serviceability of water-holding containers (χ2 = 16.56522; P < 0.001), and the difference in volume between water-holding containers was associated with the presence of Aedes spp. infection (χ2 = 4; P < 0.001), the containers up to 5 liters being the most infested. This is the first entomological research based on synanthropic mosquito breeding habitats that cover urban areas of the 3 macro-regions of the Dominican Republic.
Mosquito-borne diseases are a significant public health concern in the Caribbean. These diseases are a major challenge for health authorities as they present a practically uninterrupted transmission pattern throughout the year, becoming an obstacle to economic and social development (Alarcón-Elbal et al. 2017). In the Dominican Republic, malaria and dengue are the mosquito-borne diseases that have had more repercussions because they are endemic in the country. According to data from the Dirección General de Epidemiología/Ministerio de Salud Pública (DIGEPI/MSP 2019), the number of dengue cases in 2019 was 20,183, with 53 deaths due to this disease. This number was higher when compared with 2018, which had 1,579 cases and 1 death due to dengue. On the other hand, the number of malaria cases in 2019 was 1,302, including 4 deaths, which was higher than in 2018 that had 480 cases and no deaths. However, other diseases must also be taken into account, such as chikungunya and Zika, both of which are recent emergences in Hispaniola. Related to chikungunya, a recent study found a substantial increase in the overall mortality in the Dominican Republic during 2014, suggesting that excess deaths could have been induced by chikungunya infection and related comorbidities (Freitas et al. 2018). On the other hand, Zika virus has been linked to substantial illnesses of pregnant women and their children, stemming from the 2016–17 outbreak documented in the country (Peña et al. 2019). Lymphatic filariasis follows an endemic pattern. Although it is being considered eliminated on the island, there are still several challenges concerning its control (Gonzales et al. 2019).
Water reservoirs located inside households are preferred breeding habitats for synanthropic mosquito species (i.e., wild or free-ranging species that benefit from a shared ecology with human beings), among which Aedes aegypti (L.) and Ae. albopictus (Skuse) stand out due to their role in arbovirus transmission. Highly modified environments such as urban areas provide some advantages for these mosquito species, primarily due to the greater availability of artificial larval habitats (Derraik 2005) and complemented by poor household conditions such as inadequate water supply, and inefficient waste disposal services, among others.
Although the interest in these mosquitoes has grown in recent times due to the impact of mosquito-borne diseases in the Caribbean, there is sparse up-to-date information on mosquitoes in the Dominican Republic, except for several studies published recently in the Cibao region (Borge de Prada et al. 2018; Diéguez Fernández et al. 2019; González et al. 2019; Rodríguez Sosa et al. 2019a, 2019b). In this sense, a better knowledge of domestic breeding habitats occupied by mosquitoes would provide important epidemiological and anthropological information, with direct implications for health education, environmental awareness, and vector control.
Consequently, this study aimed to determine the microenvironmental features associated with container-dwelling mosquitoes inhabiting the domestic environment in the Dominican Republic. Ultimately, deepening the knowledge of these species is vital to develop appropriate prevention and control interventions.
MATERIALS AND METHODS
From August to September 2018, the United States Agency for International Development (USAID)-Breakthrough research project conducted a cross-sectional household survey in the Dominican Republic in provinces where educational and preventive interventions were conducted during the Zika outbreak in 2016. The Dominican Republic occupies the eastern two-thirds of Hispaniola, the second-largest island of the Greater Antilles, sharing it with Haiti and bordered by the Caribbean Sea and the Atlantic Ocean.
To increase the probability of reaching hard-to-reach populations, the evaluation team employed time–space sampling or time–location sampling (TLS) when possible. In TLS we used a sample drawn from a universe of locations, days, and times in which a population of interest is available. To avoid selection bias, provinces were randomly selected based on population density and previously reported confirmed cases of Zika virus infection.
The survey, which assessed knowledge, attitudes, and behaviors related to the prevention of Zika and other diseases transmitted by Ae. aegypti, was carried out in 9 Dominican provinces: Puerto Plata, Santiago, La Vega, Azua, San Cristóbal, La Altagracia, La Romana, Santo Domingo, and Distrito Nacional (Fig. 1). In the context of this survey on human behaviors, a parallel house-to-house mosquito breeding habitat survey was carried out in all the households visited.
Collection, processing, and identification
For sampling, trained volunteers visited the households, carefully informed the residents of the purpose and procedures of the study, and obtained informed consent from the head of the household. Volunteers were undergraduate students from medical school, and psychology department. Each group was composed of 2 volunteers with medical background, one with psychology background (responsible for conducting participants' interviews), and one supervisor. Each supervisor was capable of conducting quality controls with data collection and sampling. One senior entomologist was available to provide immediate feedback as needed. An initial training on entomological inspection was provided to all volunteers, along with interview skills to facilitate public interaction. Timetable with location distribution was assigned for a day-long inspection and interviews, lasting approximately 6–7 h. Each household inspection lasted between 20 and 30 min, based on the number and size of reservoirs inspected.
The entomological survey was carried out to detect larval breeding sites in dwellings, both in domestic areas (inside houses) and in the surrounding (peri-domestic) areas. The volunteers sampled all containers with the potential to store water and collected information on location (indoors or outdoors), type (drums, tires, bottles, cans, buckets, discarded appliances, etc.), material (plastic, metal, cement, etc.), flowers and/or vegetation (presence or absence), capacity (0–100, 101–500, 501–1,000, 1,001–5,000, >5,000 ml), and volume of stored water (0–100, 101–500, 501–1,000, 1,001–5,000, >5,000 ml). Each container was classified taking into account the serviceability reported by inhabitants. This classification resulted in 2 groups of containers, the serviceable and nonserviceable, the 1st type being represented by those recipients that serve a clear household purpose (e.g., water storage for domestic use, animal watering troughs) and the 2nd type that lacked utility (e.g., used tires, other solid waste). Each container was sampled only once (which is one of the limitations of the study), and the search continued until all containers were examined in each dwelling. In addition, some potential containers were impossible to sample due to inaccessibility, such as several rooftop water tanks. All immature stages (larvae and/or pupae) in positive containers were collected with disposable pipettes and plastic trays, and then transferred to hermetically sealed pots properly labeled before being transported to the Laboratory of Entomology, Institute for Tropical Medicine and Global Health at Universidad Iberoamericana, Santo Domingo, Dominican Republic.
At the laboratory, preimaginal stages were moved alive into mosquito breeders (Bioquip Products, Rancho Domínguez, CA) with their water for rearing; 3rd and 4th larval instars were killed by placing them in hot water (60°C) for 1 min and then preserved in labeled vials containing 70% ethanol to be ready for identification. The collected pupae were allowed to emerge into adults for taxonomic identification after being killed by placing them in a freezer for 30 min. Females were identified on the basis of morphological characters and when necessary, males were cleared in a 5% KOH solution for 6 h before their genitalia were mounted on slides in Hoyer's mounting medium. Both immature and adult mosquitoes were identified using taxonomic keys by González Broche (2006). Voucher specimens were deposited at the Laboratory of Entomology.
The entomological indicators used for the analysis were: 1) House index (HI): no. of houses infested with larvae and pupae/no. of houses inspected × 100; 2) Container index (CI): no. of containers infested with larvae and pupae/no. of containers inspected × 100; and 3) Breteau index (BI): no. of positive containers/total no. of houses inspected × 100. Finally, a novel entomological index, Ae. aegypti Breeding Percentage (BP): no. of Ae. aegypti–positive breeding sites/no. of Aedes spp.–positive breeding sites × 100, was applied (Ong et al. 2019).
Nonparametric tests were performed due to nonnormal distribution of the data. Mann–Whitney U-test was conducted to determine the influence of the presence of plants on the density of infection. Kruskal–Wallis tests were performed to compare medians between immature stages inhabiting containers, to compare the density of larvae with the type of material. All statistical tests focused on the 3 most abundant species identified: Ae. aegypti, Ae. albopictus, and Culex quinquefasciatus (Say). Container indices for the material types and volume of water holding were compared using the chi-square test. The significance level was set to alpha = 0.05. All statistical tests were analyzed using IBM SPSS 2017, Version 25.0 for Windows (IBM, Armonk, NY).
A total of 665 households were surveyed for the presence of immature mosquitoes across 30 neighborhoods belonging to 9 Dominican provinces. A total of 1,420 water-filled container habitats were examined, of which 278 (19.6%) harbored immature mosquitoes. We excluded 49 potential containers from further analysis due to logistic problems and/or inability to access. A total of 4,830 specimens (4,310 larvae and 520 pupae) of 5 species were captured: Ae. aegypti, Ae. albopictus, Cx. quinquefasciatus, Anopheles albimanus (Wied.), and Wyeomyia mitchellii (Theobald).
Immature Aedes spp. were collected in 274 water-holding containers, accounting for 19.3%. The dominance of Ae. aegypti was marked, as it was present in all sampled neighborhoods, inhabiting 272 containers (19.1%). Aedes albopictus was the second-most common species present in 3 provinces and found in 19 water-holding containers (1.3%). The remaining species were found sporadically: Cx. quinquefasciatus appeared once in La Romana and once in La Vega (cohabiting with Ae. aegypti in the latter); An. albimanus once in Azua (cohabiting with Ae. aegypti); and Wy. mitchellii once in San Cristóbal, breeding in a bromeliad. There were 24 double infestations, with Ae. aegypti and Ae. albopictus accounting for most of them (75%).
A total of 68 types of water-holding container were found, which were then categorized into 19 different groups. The most frequently found types of containers were: drums or water tanks (584; 41.1%), buckets (369; 25.9%), bottles (191; 13.4%), and plates (43; 3%), among others (Table 1). Plastic containers were the most important mosquito-breeding habitat in the survey (1,200; 84.5%), followed by metal containers (92; 6.5%), glass (59; 4.1%), cement (30; 2.1%), and rubber (12; 0.8%), among others (Table 2). By location, the province with the highest number of infested water-holding containers was San Cristóbal (78/276; 28.3%), followed by Santiago (51/324; 15.7%), and Azua (51/218; 23.4%) (Table 3).
The results of the commonly used larval indices showed the HI was the highest in Distrito Nacional (39.3%), followed by La Altagracia (35%), Azua (33.3%), San Cristóbal (30%), Puerto Plata (19.2%), and La Romana (16.7%). The CI of Aedes spp. was higher in Distrito Nacional (29%), followed by San Cristóbal (28.3%), Azua (23.4%), Santo Domingo (18.4%), and Santiago (15.7%); the lowest CI was found in La Vega (9.5%), followed by Puerto Plata (10%), La Altagracia (13%), and La Romana (13%). The BI of Aedes spp. was higher in Distrito Nacional (64.3%), followed by San Cristóbal (58.6%), Azua (58.6%), and La Altagracia (55%); the BI was lowest in La Vega (20.4%) and Santo Domingo (29.2%). Finally, the mean of the BP by province was >90% in 8 of the 9 provinces sampled, and 100% in 5 provinces (Table 3).
The serviceable water-holding containers accounted for 86% of the total containers analyzed. The presence of Aedes spp. was associated with the serviceability of the water-holding containers (χ2 = 16.56522; P < 0.001). Specifically, the odds ratio for the presence of Aedes spp. in serviceable containers was 2.8682 (P < 0.001). Regarding the container material, metal water-holding containers were not associated with the presence of Aedes spp. (P = 0.065), neither were the plastic water-holding containers (P = 0.845). The presence of containers made from polystyrene foam (P = 0.001), ceramic (P = 0.002), cement (P = 0.021), and clay P = 0.004) was associated with the presence of Aedes spp. The difference in volume between water-holding containers was associated with the presence of Aedes spp. infestation (χ2= 4; P < 0.001), with 5-liter containers being infested the most (218/275; 79.3%).
To our knowledge, this is the first entomological study based on the study of synanthropic mosquito breeding habitats that cover urban areas of the 3 macro-regions in the Dominican Republic. Similar house-to-house surveys of aedine breeding habitats have been carried out recently, although on a small geographic scale, specifically in Jarabacoa (Diéguez-Fernández et al. 2019, Rodríguez-Sosa et al. 2019a), the second-largest municipality in La Vega province.
Four of the 5 species captured in our survey have been implicated in the transmission of diseases to humans. The role of both aedine species as vectors of arboviruses has been established. During the past 50 years, Aedes-borne diseases, such as dengue, chikungunya, Zika, and even yellow fever, have emerged and/or reemerged around the world (Wilder-Smith et al. 2017). Indeed, the increasing incidence of these diseases in the 21st century has been very notable, which has coincided with a significant worldwide dispersion of vectors influenced, in turn, by factors such as climate change, elevated carbon emissions, and human population growth and international trade, among others (Kamal et al. 2018). Although rare in the domestic environment in our study, the presence of Cx. quinquefasciatus and An. albimanus should not be ignored as they are very important in the transmission of parasitic diseases in Hispaniola. Culex quinquefasciatus plays a major role in the transmission of bancroftian filariasis and West Nile virus; in fact, Hispaniola accounts for around 95% of cases of lymphatic filariasis in the Western Hemisphere and is the only remaining malaria-endemic island in the Caribbean, despite the efforts to eradicate these diseases (Gonzales et al. 2019). Furthermore, An. albimanus transmits Plasmodium falciparum (Welch) on the island, the causal agent of malaria, which becomes a life-threatening condition when treatment is not received as soon as the symptoms appear. Regarding the 5th species found in our study, although Wy. mitchellii females obtain their blood meals from warm-blooded animals, including humans, this is not a known vector of diseases to humans (Scherer et al. 1971).
In our study, the dominant mosquito species that emerged from the collected immature stages were Ae. aegypti, followed by Ae. albopictus. In relation to the resting behavior of these 2 aedines, Ae. aegypti adults are known to rest in close contact with human habitats or even indoors (Dzul-Manzanilla et al. 2017). This mosquito is considered to have adapted to the domestic environment to the point that it breeds mainly in indoor artificial water-holding containers. However, in our study Ae. aegypti was found breeding mostly in outdoors containers even though approximately one-third of the positive containers were located indoors (Tables 1 and 2). In fact, the accommodation of this species to indoor environments increases its bloodfeeding success, nuisance, and vectorial capacity. Consequently, this markedly endophilic and anthropophilic behavior make Ae. aegypti the most efficient vector of arboviruses (Dzul-Manzanilla et al. 2017). Nevertheless, it has been also reported breeding in urban solid waste in the public environment in the country (Borge de Prada et al. 2018). On the other hand, Ae. albopictus is adapted to the peri-domestic environment and is considered an exophilic species that most often rests outdoors on plant foliage and other vegetation (Samson et al. 2013), which coincides with our results since immature Ae. albopictus were only found in outdoor containers, as also reported by Rodríguez-Sosa et al. (2019a) in the Cibao region. Aedes albopictus shows an opportunistic feeding behavior on a wide range of hosts (Delatte et al. 2010), in natural habitats and outdoor man-made containers (Rodríguez-Sosa et al. 2019b).
Larvae of Cx. quinquefasciatus are occasionally found in domestic and peri-domestic water containers. However, this species breeds in a wider variety of sites such as shallow ponds, streams, water-holding bromeliads, artificial containers, and man-made impoundments, among others (Rodríguez-Sosa et al. 2019b). Moreover, its larvae are usually found in water containing high concentrations of organic detritus, which makes this species one of the few pollution-tolerant mosquito species (Clements 2000). Some studies focused on interspecific competition remark the competitive advantages of Ae. aegypti and Ae. albopictus over Cx. quinquefasciatus. While Ae. aegypti is less vulnerable to changes in temperature and more successful in exploiting microhabitats when food is scarce (Santana-Martínez et al. 2017), Ae. albopictus also seems a superior resource competitor (Allgood and Yee 2014). This asymmetrical competition may explain the scarce presence of Cx. quinquefasciatus observed in our study.
Concerning the other 2 species, Rodríguez-Sosa et al. (2019b) found An. albimanus in natural and man-made habitats of clear water in open, shallow, sunlit pools, ponds, and rarely in small artificial containers such as used tires or water-holding containers, as seen in our study where it was found only once in a drum. On the other hand, these authors found Wy. mitchellii closely associated with natural water-holding plants in forested areas.
Concerning the purpose of containers, our analysis showed that the presence of Aedes spp. was positively associated with the serviceability of the water-holding containers, i.e., serviceable containers were 1.87 times more probable to have the presence of Aedes spp. than nonserviceable ones. In fact, serviceable or useful water-holding containers accounted for 86% of the total containers analyzed. Immature Ae. aegypti mostly colonized drinking water storage containers with clean water, considering as “clean” the water that is clear, with low turbidity. This may be explained by the fact that serviceable containers store water permanently for essential use in household tasks, while those that are not useful retain water depending mostly on rainfall. This makes the former accessible for longer than the latter if appropriate preventive measures are not taken, such as the use of household bleach, application of larvicidal products, sealing of containers with lids or nets, or cleaning water storage containers regularly. In a recent study carried out in the Cibao, it was found that useful or essential containers were 54% of all those reported with the presence of larvae of Ae. aegypti (Diéguez Fernández et al. 2019). However, in our study, as in others recently carried out in the Dominican Republic (Borge de Prada et al. 2018, González et al. 2019, Rodríguez-Sosa et al. 2019a) and other Caribbean countries, Ae. aegypti has also been found breeding in containers with abundant organic matter, such as drinking troughs, solid waste, or used tires, among others. Leaf litter and algae were associated significantly with a high infestation of this vector in Puerto Rico (Barrera et al. 2006).
Our analyses revealed that water-holding containers such as drums or water tanks, buckets, gallons, and pails were consistently more likely to contain Aedes larvae; the outdoor 55-gallon drum was the most productive, and consequently the key container (Table 1). As the municipal water supply is not guaranteed all the time in most of these neighborhoods, people accumulate water mostly in drums (which are rarely covered, as we observed) for non–drinking use, and in smaller containers for drinking and cooking usually indoors.
According to the PAHO (1994), an area is considered at a high risk of transmission when these indices are above the threshold of 5% for the HI and BI, and 3% for the CI. As can be seen in Table 3, our larval indices are higher than the threshold values accepted in almost all neighborhoods visited, which suggests a very high risk of Ae. aegypti–transmitted viruses, especially in Distrito Nacional. The CIs of Azua, San Cristóbal, and Distrito Nacional (23.4%, 28.3%, and 29%, respectively) are higher than that observed in a Cibao cemetery (23.07% in the dry season, 18.7% in rainy season) where no control measures were applied (González et al. 2019).
Compared with other Caribbean studies, it can be observed that our larval indices are well over the ones obtained by Sanchez et al. (2006) in Cuba or Martín Díaz et al. (2014) in Haiti, although these studies were carried out over long periods and with the purpose to evaluate certain vector surveillance programs with an emphasis on Ae. aegypti. The total averages of our larval indices (HI = 26%, CI = 19.3%, BI = 41.8%) are also higher than that obtained by Barrera et al. (2019) in Puerto Rico before the impact of the hurricanes Irma and María (HI = 14%, CI = 3%, BI = 19%), and our CI even higher than Puerto Rico's CI after these natural disasters (HI = 33%, CI = 12%, BI = 62%). According to the BP index recently tested in Singapore, in areas where Ae. aegypti is entrenched (BP ≥ 20%), more resources should be assigned for intensive vector control (Ong et al. 2019). The BP obtained in our study (BP = 94%), together with the other indices, shows that mosquito control programs and personal protection measures at the household level are inadequate (or nonexistent) in the Dominican Republic.
However, larval indexes do not provide information about mosquitoes breeding in urban spaces that are not dwellings, such as vacant lots or accumulations of urban solid waste on roads and streams (Borge de Prada et al. 2018). Other important limitations are that these indexes depend on the visual location of the containers, which do not reflect the true prevalence of synanthropic mosquitoes due to the presence of cryptic containers such as roof gutters, catch basins, or septic tanks (Arana-Guardia et al. 2014). Taking into account the above and considering that some containers (e.g., rooftop water tanks and other containers with impossible or unsafe access) could not be sampled, the household infestation of immature Aedes reported in our study may even be underestimated. Furthermore, in our study, BP index does not appear to be very informative since most of the individuals captured belonged to the genus Aedes.
In relation to the microenvironmental features associated with synanthropic mosquitoes, specifically between type of material and infestation, polystyrene foam (P = 0.001), ceramic (P = 0.002), cement (P = 0.021), and clay water-holding containers (P = 0.004) were associated positively with the presence of Aedes spp., but not the plastic ones (P = 0.845) or metal (P = 0.065). This might be explained by an interaction between the serviceability of containers and the volume of water and material. For example, many nonserviceable containers are of plastic or metal material, and with less volume of water. Our results are in contrast with those of González et al. (2019) since they failed to show an association between material and infestation. As has been seen in other studies, Ae. aegypti showed an overall preponderance for plastic containers and flower tubs, which should be removed to reduce the Ae. aegypti population (Islam et al. 2019). In our case, no association was found with the plastic containers, neither with the presence of flowers or vegetables. In the latter, some studies show that the density of Ae. aegypti become greater in the absence of flowers, so these would act as a negative factor (González et al. 2019). This can be explained by the fact that this species is typically found in containers with clean water, and later as water becomes more organic due to flowers or vegetation, other species become predominant.
Lastly, the differences in volume between water-holding containers were associated with the presence of Aedes spp. infection. Almost a quarter (22.5%) of containers with >5 liters were infested, representing approximately 80% of all containers with the presence of Aedes spp. Although the relation between volume and infestation is not linear, it seems to respond to some disposition regarded to the mosquito reproduction. In this sense, our results are in line with the findings of Zahiri and Rau (1998), who observed that a larger volume of water increased the oviposition attraction in Ae. aegypti. In this regard, Islam et al. (2019) found that the most immature mosquito–positive containers (117; 34.31%) were medium-sized containers with volumes of 1 to <50 liters. In another report, Barrera et al. (2006) found that larvae of Ae. aegypti were significantly associated with water volume (>1.5 liters), which may reflect the combined effect of other resources and space; or conversely, the adverse effects of a small volume with excessive competitors and limited food.
To date, none of these Aedes-borne diseases has an effective vaccine, except for yellow fever. Moreover, new viruses may potentially emerge that could be transmitted by these vectors. Therefore, vector control is an essential component of the prevention and management of these diseases. For some diseases, vector is the only feasible target for control. The past decade has seen a renewed global emphasis on vector control, focusing on integrated vector management, which transforms the conventional system of control by making it more evidence based, integrated, and participative (WHO 2012). Control must be mainly achieved through eliminating larval development habitats, with the attendant use of insecticides and public education; larval control efforts invariably must focus on freshwater habitats of the 2 most synanthropic mosquito species, Ae. aegypti and Ae. albopictus.
Because Aedes mosquitoes breed in and around humans and thrive in conditions largely controlled by the public, there is a significant need for the development of community-based programs and behavior change measures to both expand and sustain current formal vector control services and operations (CARPHA 2017). In the Dominican Republic, awareness campaigns aimed at informing, sensitizing, and mobilizing communities to eliminate the risks associated with the presence of mosquito-borne diseases have historically taken place mainly during epidemic periods with no sustainability over time. The educational program, Sácale los pies al mosquito, for the prevention and control of mosquito-borne diseases in Jarabacoa, has been the first in providing key elements to promote the optimal participation of neighborhoods and communities in the prevention and control of this problem, as well as ensuring the sustainability of the actions developed (Vásquez Bautista et al. 2019).
The Dominican Republic has been historically affected by mosquito-borne infectious diseases; unfortunately, programs aimed to monitor and surveil viral and mosquito interaction and circulation are still nonexistent. Investment from national resources for these projects is cumbersome and requires a more systemic approach. It should not be forgotten that, as a tourist-attracting nation, the country could play a significant role in the global transmission of arbovirus (Ozawa et al. 2018). Besides, an epidemic will result in increased medical costs and have implications for the economy and tourism.
The importance of emerging and reemerging pathogens today should be considered in all future planning. The age of emerging pathogens is a continuous pattern that never stops; we are called to be prepared for the next pandemic.
We thank the team of volunteers from Universidad Iberoamericana, the administrative and financial department, and all participants who spontaneously collaborated and allowed the team of researchers to do data and specimen collection. We also thank the anonymous reviewers for their valuable comments on our manuscript. This project was partially funded by a collaborative agreement between Tulane University (principal Recipient from the United States Agency for International Development [USAID]-Breakthrough Project) and Universidad Iberoamericana under the number AID-OAAA-A-17-00018.